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Physiological response of the green microalgae Dunaliella tertiolecta against imidazolium ionic liquids [bmim][BF4] and/or [omim][BF4]: the role of salinity on the observed effects

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Abstract

The ability of two widely used imidazolium-based ionic liquids (ILs) to affect the physiological behavior of the green alga Dunaliella tertiolecta treated in culture media with different salinities (30 and 35 ‰) was investigated. Algae species were exposed to 1-butyl-3-methylimidazolium tetrafluoroborate ([bmim][BF4]), 1-octyl-3-methylimidazolium tetrafluoroborate ([omim][BF4]), and their binary mixture [bmim][BF4]–[omim][BF4] (ratio 1:1) for 96 h, in f/2 medium with different salinities (30 and 35 ‰). Every 24 h, the growth rate (μ) and the percent inhibition (% I) as well as the concentrations of carotenoids (in terms of carotene content) and chlorophyll a (Chl a) were determined. According to the results, the culture media salinity plays a key role in IL-mediated inhibitory effects on algae. In both salinities, ILs can act against algal growth rate rather than Chl a synthesis, merely due to the existence of a cross-linking with carotenoids, whose enhancement prior or in parallel with Chl a synthesis could play an important role against their growth restriction.

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References

  • Aminot A, Ray F (2000) Standard procedures for the determination of chlorophyll a by spectroscopic methods. ICES Tech Mar Environ Sci 30:1–18

    Google Scholar 

  • APHA (1989) Toxicity testing with phytoplankton. Standard methods for examination of water and wastewater, 17th Ed, Suppl. Washington, DC, USA.

  • APHA (1996) Standard methods for the examination of water and wastewater. 20th Ed. Am. Pub. Health Assoc, Washington, DC. USA

    Google Scholar 

  • Aravantinou AF, Tsarpali V, Dailianis S, Manariotis ID (2015) Effect of cultivation media on the toxicity of ZnO nanoparticles to freshwater and marine microalgae. Ecotox Environ Safe 114:109–116

    Article  CAS  Google Scholar 

  • ASTM (American Society for Testing and Materials) (1996) Standard guide for conducting static 96-h toxicity tests with microalgae. Vol. 11.05. ASTM, West Conshohocken, PA. USA

    Google Scholar 

  • Bae MJ, Park YS (2014) Biological early warning system based on the responses of aquatic organisms to disturbances: a review. Sci Total Environ 466–467:635–649

    Article  PubMed  Google Scholar 

  • Ben-Amotz A, Polle JEW, Subba Rao DV (eds) (2009) The alga Dunaliella: biodiversity, physiology, genomics and biotechnology. Science Publishers, Enfield

    Google Scholar 

  • Bernot RJ, Kennedy EE, Lamberti GA (2005) Effects of ionic liquids on the survival, movement and feeding behavior of the freshwater snail, Physa acuta. Environ Toxicol Chem 24:1759–1765

    Article  CAS  PubMed  Google Scholar 

  • Boyle TP (1984) The effect of environmental contaminants on aquatic algae. In: Shubert LE (ed) Algae as ecological indicators. Academic Press, New York, pp 237–256

    Google Scholar 

  • Cammarata L, Kazarian SG, Salterb PA, Welton T (2001) Molecular states of water in room temperature ionic liquids. Phys Chem Chem Phys 3:5192–5200

    Article  CAS  Google Scholar 

  • Campanella L, Cubadda F, Sammartino MP, Saoncella A (2000) An algal biosensor for the monitoring of water toxicity in estuarine environments. Water Res 25:69–76

    Google Scholar 

  • Cantrell A, McGarvey DJ, Truscott TG, Rancan F, Böhm F (2003) Singlet oxygen quenching by dietary carotenoids in a model membrane environment. Arch Biochem Biophys 412:47–54

    Article  CAS  PubMed  Google Scholar 

  • Cho CW, Pham TPT, Jeon YC, Vijayaraghavan K, Choed WS, Yun YS (2007) Toxicity of imidazolium salt with anion bromide to a phytoplankton Selenastrum capricornutum: effect of alkyl-chain length. Chemosphere 69:1003–1007

    Article  CAS  PubMed  Google Scholar 

  • Cvjetko Bubalo MC, Radošević K, Redovniković IR, Halambek J, Srček VG (2014) A brief overview of the potential environmental hazards of ionic liquid. Ecotoxicol Environ Saf 99:1–12

    Article  CAS  Google Scholar 

  • Del Campo JA, Garcia-Gonzalez M, Guerrero MG (2007) Outdoor cultivation of microalgae for carotenoid production: current state and perspectives. Appl Microbiol Biot 74:1163–1174

    Article  CAS  Google Scholar 

  • DeLorenzo AM (2009) Utility of Dunaliella in ecotoxicity testing. In: Ben-Amotz A, Polle JEW, Rao DVS (eds) The alga Dunaliella: biodiversity, physiology, genomics and biotechnology. Science Publishers, Enfield, pp 495–512

    Chapter  Google Scholar 

  • Docherty KM, Kulpa CFJ (2005) Toxicity and antimicrobial activity of imidazolium and pyridinium ionic liquids. Green Chem 7:185–189

    Article  CAS  Google Scholar 

  • El-Sheekh MM, El-Naggar AH, Osman MEH, El-Mazaly E (2003) Effect of cobalt on growth, pigments and the photosynthetic electron transport in Monoraphidium minutum and Nitzchia perminuta. Braz J Plant Physiol 15:159–166

    Article  CAS  Google Scholar 

  • Freire MG, Santos LMNBF, Fernandes AM, Coutinho JAP, Marrucho IM (2007) An overview of the mutual solubilities of water–imidazolium-based ionic liquids systems. Fluid Phase Equilibr 261:449–454

    Article  CAS  Google Scholar 

  • Garcia-Gonzalez M, Moreno J, Manzano JC, Florencio FJ, Guerrero MG (2005) Production of Dunaliella salina biomass rich in 9-cis-β-carotene and lutein in a closed tubular photobioreactor. J Biotechnol 115:81–90

    Article  CAS  PubMed  Google Scholar 

  • Grishina EP, Ramenskaya LM, Gruzdev MS, Kraeva OV (2013) Water effect on physicochemical properties of 1-butyl-3-methylimidazolium based ionic liquids with inorganic anions. J Mol Liq 177:267–272

    Article  CAS  Google Scholar 

  • Jeffrey SW, Skarstad E (2009) Pigments of green and red forms of Dunaliella, and related chlorophytes. In: Ben-Amotz A, Polle JEW, Rao DVS (eds) The alga Dunaliella: biodiversity, physiology, genomics and biotechnology. Science Publishers, Enfield, pp 111–145

    Chapter  Google Scholar 

  • Jimenez C, Pick U (1993) Differential reactivity of β-carotene isomers from Dunaliella bardawil toward oxygen radicals. Plant Physiol 101:385–390

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kramer NI, Krismartina M, Rico-Rico A, Blaauboer BJ, Hermens JLM (2012) Quantifying processes determining the free concentration of phenanthrene in basal cytotoxicity assay. Chem Res Toxicol 25:436–445

    Article  CAS  PubMed  Google Scholar 

  • Kulacki KJ, Lamberti GA (2008) Toxicity of imidazolium ionic liquids to freshwater algae. Green Chem 10:104–110

    Article  CAS  Google Scholar 

  • Kumar M, Kumari P, Gupta V, Anisha PA, Reddy CRK, Jha B (2010) Differential responses to cadmium induced oxidative stress in marine macroalga Ulva lactuca (Ulvales, Chlorophyta). Biometals 23:315–325

    Article  CAS  PubMed  Google Scholar 

  • Kumar M, Trivedi N, Reddy CRK, Jha B (2011) Toxic effects of imidazolium ionic liquids on the green seaweed Ulva lactuca: oxidative stress and DNA damage. Chem Res Toxicol 24:1882–1890

  • Latała A, Stepnowski P, Nędzi M, Mrozik W (2005) Marine toxicity assessment of imidazolium ionic liquids: acute effects on the Baltic algae Oocystis submarina and Cyclotella meneghiniana. Aquat Toxicol 73:91–98

    Article  PubMed  Google Scholar 

  • Latała A, Nędzi M, Stepnowski P (2009) Toxicity of imidazolium and pyridinium based ionic liquids towards algae. Chlorella vulgaris, Oocystis submarina (green algae) and Cyclotella meneghiniana, Skeletonema marinoi (diatoms). Green Chem 11:580–588

    Article  Google Scholar 

  • Latała A, Nędzi M, Stepnowski P (2010) Toxicity of imidazolium ionic liquids towards algae. Influence of salinity variations. Green Chem 12:60–64

    Article  Google Scholar 

  • Li X, Ping X, Xiumei P, Zhenbin W, Liqiang X (2005) Toxicity of cypermethrin on growth, pigments, and superoxide dismutase of Scenedesmus obliquus. Ecotoxicol Environ Saf 60:188–192

    Article  CAS  PubMed  Google Scholar 

  • Li H, Yu C, Chen R, Li J, Li J (2012) Novel ionic liquid-type Gemini surfactants: synthesis, surface property and antimicrobial activity, colloids and surfaces. Colloids Surf A 395:116–124

    Article  CAS  Google Scholar 

  • Ma JM, Cai LL, Zhang BJ, Hu LW, Li XY, Wang JJ (2010) Acute toxicity and effects of 1-alkyl-3-methylimidazolium bromide ionic liquids on green algae. Ecotoxicol Environ Saf 73:1465–1469

    Article  CAS  PubMed  Google Scholar 

  • Matzke M, Stolte S, Thiele K, Juffernholz T, Arning J, Ranke J, Welz-Biermann U, Jastorff B (2007) The influence of anion species on the toxicity of 1-alkyl-3-methylimidazolium ionic liquids observed in an (eco)toxicological test battery. Green Chem 9:1198–1207

    Article  CAS  Google Scholar 

  • Melegari SP, Perreault F, Costa RHR, Popovic R, Matias WG (2013) Evaluation of toxicity and oxidative stress induced by copper oxide nanoparticles in the green alga Chlamydomonas reinhardtii. Aquat Toxicol 142–143:431–440

    Article  PubMed  Google Scholar 

  • Nikookar K, Moradshahi A, Hosseini L (2005) Physiological responses of Dunaliella salina and Dunaliella tertiolecta to copper toxicity. Biomol Eng 22:141–146

    Article  CAS  PubMed  Google Scholar 

  • Niyogi KK (2000) Safety valves for photosynthesis. Curr Opin Plant Biol 3:455–460

    Article  CAS  PubMed  Google Scholar 

  • OECD (2011) Test no. 201: freshwater alga and cyanobacteria, growth inhibition test, OECD Guidelines for the Testing of Chemicals, Section 2, OECD Publishing, Paris. DOI: http://dx.doi.org/10.1787/9789264069923-en

  • Oren A (2005) A hundred years of Dunaliella research: 1095-2005. Sal Systems 1:2. doi:10.1186/1746-1448-1-2

  • Oukarroum A, Bras S, Perreault F, Popovic R (2012) Inhibitory effects of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Ecotoxicol Environ Saf 78:80–85

    Article  CAS  PubMed  Google Scholar 

  • Perreault F, Matias MS, Oukarroum A, Matias WG, Popovic R (2012) Okadaic acid inhibits cell growth and photosynthetic electron transport in the alga Dunaliella tertiolecta. Sci Total Environ 414:198–204

    Article  CAS  PubMed  Google Scholar 

  • Petkovic M, Seddon KR, Rebelo LPN, Silva Pereira C (2011) Ionic liquids: a pathway to environmental acceptability. Chem Soc Rev 40:1383–1403

    Article  CAS  PubMed  Google Scholar 

  • Pham TPT, Cho CW, Min J, Yun YS (2008) Alkyl-chain length effects of imidazolium and pyridinium ionic liquids on photosynthetic response of Pseudokirchneriella subcapitata. J Biosci Bioeng 105:428–428

    Google Scholar 

  • Pham TPT, Cho CW, Yun YS (2010) Environmental fate and toxicity of ionic liquids: a review. Water Res 44:352–372

    Article  CAS  PubMed  Google Scholar 

  • Ranke J, Mőlter K, Stock F, Bottin-Weber U, Poczobutt J, Hoffmann J, Ondruschka B, Filser J, Jastorff B (2003) Biological effects of imidazolium ionic liquids with varying chain lengths in acute Vibrio fischeri and WST-1 cell viability assays. Ecotoxicol Environ Saf 28:396–404

    Google Scholar 

  • Saha S, Hamaguchi HO (2006) Effect of water on the molecular structure and arrangement of nitrile-functionalized ionic liquids. J Phys Chem B 110:2777–2781

    Article  CAS  PubMed  Google Scholar 

  • Samori C, Malferrari D, Valbonesi P, Montecavalli A, Moretti F, Galletti P, Sartor G, Tagliavini E, Fabbri E, Pasteris A (2010) Introduction of oxygenated side chain into imidazolium ionic liquids: evaluation of the effects at different biological organization levels. Ecotoxicol Environ Saf 73:1456–1464

    Article  CAS  PubMed  Google Scholar 

  • Shaish A, Ben-Amotz A, Avron M (1992) Biosynthesis of β-carotene in Dunaliella. Methods Enzymol 213:439–444

    Article  CAS  Google Scholar 

  • Shimizu K, Gomes MFC, Pádua AAH, Rebelo LPN, Lopes JNC (2010) Three commentaries on the nano-segregated structure of ionic liquids. J Mol Struc-Theochem 946:70–76

    Article  CAS  Google Scholar 

  • Stepnowski P, Składanowski AC, Ludwiczak A, Łączyńska E (2004) Evaluating the cytotoxicity of ionic liquids using human cell line HeLa. Hum Exp Toxicol 23:513–517

    Article  CAS  PubMed  Google Scholar 

  • Takaichi S (2011) Carotenoids in algae: distributions, biosyntheses and functions. Mar Drugs 9:1101–1118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Telfer A (2002) What is β-carotene doing in the photosystem II reaction centre? Phil Trans R Soc B 357:1431–1439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsarpali V, Dailianis S (2015) Toxicity of two imidazolium ionic liquids, [bmim][BF4] and [omim][BF4], to standard aquatic test organisms: role of acetone in the induced toxicity. Ecotoxicol Environ Saf 117:62–71

    Article  CAS  PubMed  Google Scholar 

  • Tsiaka P, Tsarpali V, Ntaikou I, Kostopoulou MN, Lyberatos G, Dailianis S (2013) Carbamazepine-mediated pro-oxidant effects on the unicellular marine algal species Dunaliella tertiolecta and the hemocytes of mussel Mytilus galloprovincialis. Ecotoxicology 22:1208–1220

    Article  CAS  PubMed  Google Scholar 

  • U.S. EPA (U.S. Environmental Protection Agency) (1974) Marine algal assay procedure bottle test: eutrophication and lake restoration. Branch National Environmental Research Center, Corvallis, OR, USA

  • Ventura SPM, Gonçalves AMM, Gonçalves F, Coutinho JAP (2010) Assessing the toxicity on [C3mim][Tf2N] to aquatic organisms of different trophic levels. Aquat Toxicol 96:290–297

    Article  CAS  PubMed  Google Scholar 

  • Ventura SPM, Gurbisz M, Ghavre M, Ferreira FMM, Gonçalves F, Beadham I, Quilty B, Coutinho JAP, Gathergood N (2013) Imidazolium and pyridinium ionic liquids from mandelic acid derivatives: synthesis and bacteria and algae toxicity evaluation. ACS Sustain Chem Eng 1:393–402

    Article  CAS  Google Scholar 

  • Wasserscheid P, Keim W (2000) Ionic liquids-new “solutions” for transition metal catalysis. Angew Chem Int Ed 39:3772–3789

    Article  CAS  Google Scholar 

  • Wong PK (2000) Effects of 2, 4-D, glyphosate and paraquat on growth, photosynthesis and chlorophyll-a synthesis of Scenedesmus quadricauda Berb 614. Chemosphere 4:177–182

    Article  Google Scholar 

  • Woodall AA, Britton G, Jackson MJ (1997) Carotenoids and protection of phospholipids in solution or in liposomes against oxidation by peroxyl radicals: relationship and protective ability. Biochim Biophys Acta 7:617–635

    Google Scholar 

  • Zhang C, Malhotra SV, Francis AJ (2011) Toxicity of imidazolium- and pyridinium-based ionic liquids and the co-metabolic degradation of N-ethylpyridinium tetrafluoroborate. Chemosphere 82:1690–1695

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by the annual research grant sanctioned to the Section of Animal Biology by the University of Patras, Greece. The present work is included in the doctoral thesis of Ms. V. Tsarpali. Further data associated with the current article can be found within the supplementary file.

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  1. Section of Animal Biology, Department of Biology, Faculty of Sciences, University of Patras, 26500, Patras, Greece

    Vasiliki Tsarpali, Kassiani Harbi & Stefanos Dailianis

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  1. Vasiliki Tsarpali
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  2. Kassiani Harbi
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  3. Stefanos Dailianis
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Correspondence to Stefanos Dailianis.

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Tsarpali, V., Harbi, K. & Dailianis, S. Physiological response of the green microalgae Dunaliella tertiolecta against imidazolium ionic liquids [bmim][BF4] and/or [omim][BF4]: the role of salinity on the observed effects. J Appl Phycol 28, 979–990 (2016). https://doi.org/10.1007/s10811-015-0613-6

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